Genomic Organization and Evolution of the Atlantic salmon Hemoglobin Repertoire

Background: The genomes of salmonids are considered pseudo-tetraploid undergoing reversion to a stable diploidstate. Given the genome duplication and extensive biological data available for salmonids, they are excellent modelorganisms for studying comparative genomics, evolutionary processes, fates of duplicated genes and the geneticand physiological processes associated with complex behavioral phenotypes. The evolution of the tetrapodhemoglobin genes is well studied; however, little is known about the genomic organization and evolution of teleosthemoglobin genes, particularly those of salmonids. The Atlantic salmon serves as a representative salmonid speciesfor genomics studies. Given the well documented role of hemoglobin in adaptation to varied environmentalconditions as well as its use as a model protein for evolutionary analyses, an understanding of the genomic structureand organization of the Atlantic salmon a and b hemoglobin genes is of great interest.Results: We identified four bacterial artificial chromosomes (BACs) comprising two hemoglobin gene clustersspanning the entire a and b hemoglobin gene repertoire of the Atlantic salmon genome. Their chromosomallocations were established using fluorescence in situ hybridization (FISH) analysis and linkage mapping,demonstrating that the two clusters are located on separate chromosomes. The BACs were sequenced andassembled into scaffolds, which were annotated for putatively functional and pseudogenized hemoglobin-likegenes. This revealed that the tail-to-tail organization and alternating pattern of the a and b hemoglobin genes arewell conserved in both clusters, as well as that the Atlantic salmon genome houses substantially more hemoglobingenes, including non-Bohr b globin genes, than the genomes of other teleosts that have been sequenced.Conclusions: We suggest that the most parsimonious evolutionary path leading to the present organization of theAtlantic salmon hemoglobin genes involves the loss of a single hemoglobin gene cluster after the whole genomeduplication (WGD) at the base of the teleost radiation but prior to the salmonid-specific WGD, which thenproduced the duplicated copies seen today. We also propose that the relatively high number of hemoglobingenes as well as the presence of non-Bohr b hemoglobin genes may be due to the dynamic life history of salmonand the diverse environmental conditions that the species encounters.Data deposition: BACs S0155C07 and S0079J05 (fps135): GenBank GQ898924; BACs S0055H05 and S0014B03(fps1046): GenBank GQ898925